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    9 Uveitis and Ocular Inflammation

    Chapter 11: Infectious Uveitis: Nonbacterial Causes

    Protozoal Uveitis

    Toxoplasmosis

    Toxoplasmosis is the most common cause of infectious posterior uveitis in adults and children. It is caused by the parasite Toxoplasma gondii, a single-cell obligate intracellular apicomplexan parasite with a worldwide distribution (Fig 11-26). Felines are the definitive hosts of T gondii, and humans and a variety of other animals serve as intermediate hosts. T gondii has a complex life cycle and exists in 3 major forms:

    • the oocyst, or soil form (10–12 μm), which contains sporozoites

    • the tachyzoite, or infectious form (4–8 μm)

    • the tissue cyst, or latent form (10–200 μm), which contains as many as 3000 bradyzoites

    Transmission of T gondii to humans and other animals may occur with all 3 forms of the parasite through a variety of vectors. The oocysts reproduce in the cat intestine and are shed in feces, contaminating the environment. After maturation in the soil, these oocysts may then be ingested by intermediate hosts. Tachyzoites, the proliferative form of the parasite, are found in the circulatory system and may invade nearly all host tissue. In an immunocompetent host, tachyzoites proliferation eventually stops. However, some micro-organisms may persist as dormant bradyzoites within intercellular tissue cysts.

    Figure 11-26 Histology of Toxoplasma gondii infection of the retina. Note the cysts (arrows) in the necrotic retina.

    As of this writing, the CDC estimates that 11% of the United States population age 6 and older has been infected with T gondii. Of that group, 2% may develop ocular toxoplasmosis. The reported seropositivity rates among healthy adults vary considerably worldwide. An estimated 80% of the population in southern Brazil is infected with T gondii, and up to 18% of these individuals may develop eye disease. Some studies show a greater genotypic heterogeneity of parasites in Brazil than in North America. Such differences may contribute to variance in disease severity and ocular involvement in different regions of the world.

    Human infection by T gondii may be either acquired or congenital. The principal modes of transmission include

    • ingestion of undercooked, infected meat containing tissue cysts

    • ingestion of contaminated water, fruit, or vegetables with oocysts

    • inadvertent contact with cat feces, cat litter, or soil containing oocysts

    • transplacental transmission with primary infection during pregnancy

    • blood transfusion or organ transplantation

    Five of the epidemics that occurred between 1979 and 2003 have been well studied, and contaminated water supplies or inhaled/ingested sporulated oocysts in dirt were implicated as sources of infection.

    Data collected from the 2009–2010 National Health and Nutrition Examination Survey (NHANES) study shows an age-adjusted seroprevalence among women of childbearing age (15–44 years) of 9.1% in the United States population. Thus, most women of childbearing age in the United States are susceptible to T gondii infection. The American Academy of Pediatrics estimates that the incidence of primary infection during pregnancy in the United States is approximately 0.2–1.1 per 1000 pregnant women, translating to 800–4400 women per year with acute T gondi infection during the 4 million yearly pregnancies in the U.S.

    Overall, 40% of primary maternal infections result in congenital infection; transplacental transmission is highest during the third trimester. The risk of severe disease developing in the fetus is inversely proportional to gestational age. Disease acquired early in pregnancy may result in spontaneous abortion, stillbirth, or severe congenital disease. Disease acquired later in gestation may produce an asymptomatic, normal-appearing infant with latent infection. Chronic or recurrent maternal infection during pregnancy is not thought to confer a significant risk of congenital toxoplasmosis because maternal immunity protects against fetal transmission. However, congenital toxoplasmosis may occur in an immune pregnant mother reinfected with a new, more virulent strain.

    Pregnant women without serologic evidence of T gondii infection should be advised to take the following precautions:

    • Avoid ingestion of raw/undercooked meat (freezing at −20°C/−4°F overnight also destroys tissue cysts).

    • Drink only well-filtered or boiled water.

    • Carefully wash vegetables and fruits before consumption.

    • Use gloves and wash hands and kitchen utensils well after handling meat or soil.

    • Avoid contact with felines and their feces (including in soil or litter boxes).

    The classic presentation of congenital toxoplasmosis, which includes retinochoroiditis, hydrocephalus or microcephaly, intracranial calcifications, and cognitive impairment (Sabin’s tetrad), occurs in less than 10% of infected children. Retinochoroidal lesions, found in up to 80% of cases, are the most common abnormality in patients with congenital toxoplasmosis. Lesions are bilateral in approximately 85% of affected individuals and carry a predilection for the posterior pole and macula (Fig 11-27). Posterior segment involvement may be subclinical and chronic. As many as 85% of infected children develop retinochoroiditis after a mean of 3.7 years, and 25% of these become blind in 1 or both eyes. Most experts recommend antiparasitic therapy for newborns with congenital toxoplasmosis during the first year of life to reduce disease burden, regardless of the presence of ocular and/or systemic signs.

    Although toxoplasmosis after infancy was previously considered exclusively congenital disease reactivation, it is now recognized that ocular toxoplasmosis in children and adults may represent newly acquired infection in a significant proportion of cases. In one study, acquired postnatal infection was thought to represent up to two-thirds of cases of toxoplasmic ocular disease.

    Although dependent on the location of the lesion, presenting symptoms frequently include unilateral blurred or hazy vision and floaters. A mild to moderate granulomatous anterior uveitis is often observed, and up to 20% of patients have acutely elevated IOP at presentation. Classically, ocular toxoplasmosis appears as a focal, white retinochoroiditis, with overlying moderate vitreous inflammation (“headlight in the fog”), often adjacent to a pigmented retinochoroidal scar (Figs 11-28, 11-29). These lesions occur more commonly in the posterior pole but are occasionally found immediately adjacent to or directly involving the optic nerve; they may be mistaken for optic neuritis. Retinal vessels in the vicinity of an active lesion may show perivasculitis with diffuse venous sheathing and segmental arterial plaques (Kyrieleis arteriolitis). Vascular occlusions may also be present. Additional ocular complications include cataract, persistent vitreous opacities, macular edema, retinal detachment, epiretinal membranes, optic atrophy, and CNV. Recently acquired disease often presents as a focal retinochoroiditis in the absence of a retinochoroidal scarring (Fig 11-30).

    Figure 11-27 Fundus photograph of quiescent, partially pigmented, congenital toxoplasmic macular scar. Patient has 20/400 visual acuity.

    (Courtesy of John D. Sheppard Jr, MD.)

    Retinochoroiditis developing in immunocompromised and older patients may present with atypical findings, including large, multiple, and/or bilateral lesions, with or without associated retinochoroidal scars. This more severe clinical picture can also occur in patients receiving steroids without concomitant antiparasitic therapy (Fig 11-31). Ocular toxoplasmosis may simulate herpetic ARN. Other atypical presentations include neuroretinitis, punctate outer retinal toxoplasmosis (PORT), unilateral pigmentary retinopathy simulating retinitis pigmentosa, and other forms of intraocular inflammation in the absence of retinochoroiditis. Characteristics of PORT include small, multifocal lesions at the level of the outer retina, with exudation to subretinal space and scant overlying vitreal inflammation (Fig 11-32).

    Figure 11-28 Toxoplasmic retinochoroiditis. Fundus photograph showing intense focal retinitis with dense overlying vitritis, producing a “headlight in the fog” appearance.

    Figure 11-29 Toxoplasmosis. Fundus photograph showing satellite retinochoroiditis around an old scar.

    Figure 11-30 Fundus photograph showing toxoplasmic retinochoroiditis in the absence of a previous chorioretinal scar.

    (Courtesy of Greg Kokame, MD, and the Retina Image Bank, American Society of Retina Specialists.)

    • Centers for Disease Control and Prevention; Division of Parasitic Diseases and Malaria. Toxoplasmosis. Available at www.cdc.gov/dpdx/toxoplasmosis/. Accessed October 5, 2018.

    • Holland GN. Ocular toxoplasmosis: a global reassessment. Part I: epidemiology and course of disease. Am J Ophthalmol. 2003;136(6):973–988.

    • Holland GN. Ocular toxoplasmosis: a global reassessment. Part II: disease manifestations and management. Am J Ophthalmol. 2004;137(1):1–17.

    • Jones JL, Bonetti V, Holland GN, et al. Ocular toxoplasmosis in the United States: recent and remote infections. Clin Infect Dis. 201515;60(2):271–273.

    • Maldonado YA, Read JS; AAP Committee on Infectious Diseases. Diagnosis, treatment, and prevention of congenital toxoplasmosis in the United States. Pediatrics. 2017;139(2): e20163860.

    • Vasconcelos-Santos DV. Ocular manifestations of systemic disease: toxoplasmosis. Curr Opin Ophthalmol. 2012;23(6):543–550.

    Figure 11-31 Toxoplasmosis. Fundus photograph showing widespread retinal necrosis following periocular corticosteroid injection.

    (Courtesy of E. Mitchel Opremcak, MD.)

    Figure 11-32 Fundus photograph showing punctate outer retinal toxoplasmosis.

    (Courtesy of E. Mitchel Opremcak, MD.)

    Diagnosis

    In most cases, toxoplasmic retinochoroiditis is clinically diagnosed on the basis of the characteristic fundus lesion. Positive serologic testing for anti–T gondii IgG or IgM confirms exposure to the parasite. IgG antibodies appear after the first 2 weeks of infection, typically remain detectable for life at variable levels, and cross the placenta. IgM antibodies, however, increase in number early during the acute phase of the infection, typically remain detectable for less than 1 year, and do not cross the placenta. The presence of anti–T gondii IgG antibodies supports the diagnosis of toxoplasmic retinochoroiditis in the appropriate clinical context, whereas a negative antibody titer essentially rules out the diagnosis.

    The presence of IgM in newborns confirms congenital infection and indicates acquired disease in adults. In cases of diagnostic uncertainty, PCR testing of aqueous humor and vitreous fluid may be performed.

    • Montoya JG, Parmley S, Liesenfeld O, Jaffe GJ, Remington JS. Use of the polymerase chain reaction for diagnosis of ocular toxoplasmosis. Ophthalmology. 1999;106(8):1554–1563.

    Treatment

    Ocular toxoplasmosis is a progressive and recurrent disease. New lesions may occur at the margins of old scars as well as elsewhere in the fundus, and toxoplasmic cysts may be present in a normal-appearing retina. In the immunocompetent patient, the disease can have a self-limiting course. The borders of the lesions become sharper and less edematous over a 6–8-week period without treatment, and RPE hyperplasia occurs gradually over a period of months. In the immunocompromised patient, the disease is often more severe and progressive. Treatment can shorten the duration of parasitic replication, leading to more rapid cicatrization and ultimately a smaller retinochoroidal scar. Treatment may also reduce the frequency of inflammatory recurrences and minimize structural complications associated with intraocular inflammation.

    Numerous medications may be used to treat toxoplasmosis, and there is no consensus as to the most efficacious regimen. Most antibiotic agents have efficacy against the active tachyzoite, not the tissue-encysted bradyzoite. Little firm evidence exists that antimicrobial therapy alters the natural history of toxoplasmic retinochoroiditis in immunocompetent patients. Some clinicians may elect to observe small lesions in the retinal periphery that are not associated with a significant decrease in vision or vitritis; others treat virtually all patients in an effort to reduce the number of subsequent recurrences. Relative treatment indications include

    • lesions threatening the optic nerve or fovea

    • decreased visual acuity

    • lesions associated with moderate to severe vitreous inflammation

    • lesions greater than 1 disc diameter in size

    • persistence of disease for more than 1 month

    • presence of multiple active lesions

    Treatment is indicated in immunocompromised patients (those with HIV/AIDS, with neoplastic disease, or undergoing IMT), patients with congenital toxoplasmosis, and pregnant women with recently acquired disease.

    The classic regimen for the treatment of ocular toxoplasmosis consists of 4–8 weeks of pyrimethamine (loading dose, 50–100 mg; treatment dose, 25–50 mg/day) and sulfadiazine (treatment dose, 1 g, 4 times/day). Pyrimethamine has recently become prohibitively expensive. Folinic acid (5–10 mg/day) is added to prevent myelosuppression (leukopenia and/or thrombocytopenia), which may result from pyrimethamine therapy. A complete blood count may be checked approximately every 2 weeks during therapy. Potential adverse effects of sulfa compounds include skin rash, gastrointestinal intolerance, crystalluria, kidney stones, and Stevens-Johnson syndrome. Clindamycin (300 mg, 4 times/day) may be added to the above regimen or substituted for sulfadiazine in the case of sulfa allergy. Clindamycin, either alone or in combination with other drugs, has been effective in managing acute lesions, but pseudomembranous colitis is a potential complication. Azithromycin (500 mg daily) or atovaquone (750 mg, 2–4 times/day) may take the place of sulfadiazine or clindamycin.

    Many ophthalmologists utilize trimethoprim-sulfamethoxazole (160 mg/800 mg, 2 times/day) because of its accessibility, simplicity of administration, and cost. Clindamycin (1 mg/0.1 mL) may also be intravitreally injected in an off-label fashion, either in combination with systemic therapy or as monotherapy in patients who do not tolerate systemic therapy.

    Systemic corticosteroids (approximately 0.25–0.75 mg/kg, typically not to exceed 60 mg/day) may be considered after 48 hours of antimicrobial therapy in immunocompetent patients. The use of systemic corticosteroids without appropriate antimicrobial coverage or the use of long-acting periocular and intraocular corticosteroid formulations such as triamcinolone acetonide is contraindicated because of the potential for severe panophthalmitis and loss of the eye (see Fig 11-31). Topical corticosteroids, however, are used liberally in the presence of prominent anterior segment inflammation. Systemic corticosteroid treatment may be used for 3–5 weeks, at which time inflammation begins to subside and the retinal lesion shows signs of early cicatrization. Antimicrobial coverage should be continued for the entire period of systemic corticosteroid use.

    Newborns with congenital toxoplasmosis are commonly treated with pyrimethamine and sulfonamides (plus folinic acid) for 1 year, in consultation with a specialist in pediatric infectious diseases.

    In cases of newly acquired toxoplasmosis during pregnancy, treatment is given to prevent infection of the fetus and limit fetal damage if infection has already occurred, as well as to limit the destructive sequelae of intraocular disease in the mother. Spiramycin (treatment dose, 400 mg 3 times/day) reduces the rate of tachyzoite transmission to the fetus and may be used safely without undue risk of teratogenicity. Because this drug is commonly unavailable in the United States, alternative medications may be needed; options include azithromycin, clindamycin, and atovaquone (treatment dose, 750 mg every 6 hours). Sulfonamides may be used safely in the first 2 trimesters of pregnancy. Alternatively, intravitreal injection of clindamycin and short-acting periocular corticosteroids (eg, dexamethasone) may be utilized in pregnant women to reduce systemic adverse effects.

    Patients with HIV/AIDS require extended systemic treatment given the frequent association of ocular disease with cerebral involvement (56%) and the frequency of recurrent ocular disease when antitoxoplasmic medication is discontinued (Fig 11-33). The best regimen for secondary prophylaxis remains to be determined; however, atovaquone acts synergistically with pyrimethamine and sulfadiazine and thus may be useful for reducing the dose and toxicity of these drugs in the treatment of patients with AIDS and toxoplasmosis. The management of ocular toxoplasmosis in association with HIV/AIDS is also covered in Chapter 15.

    Figure 11-33 Enhanced computed tomography scan revealing a cerebellar lesion caused by central nervous system toxoplasmosis in a patient with AIDS who presented with ataxia.

    (Courtesy of John D. Sheppard Jr, MD.)

    Long-term intermittent trimethoprim-sulfamethoxazole treatment (160 mg/800 mg 3 times per week) was shown to decrease the risk of reactivation among patients with recurrent toxoplasmic retinochoroiditis observed over a 20-month period. A similar strategy may be useful as prophylaxis in patients with ocular toxoplasmosis and HIV/AIDS.

    Similarly, the utility of prophylactic antimicrobial treatment shortly before and after intraocular surgery in patients with inactive toxoplasmic scars—particularly scars that threaten the optic disc or fovea—was raised by a report that describes an association between cataract surgery and an increased risk of reactivation of otherwise inactive toxoplasmic retinochoroiditis. There is, however, no consensus with respect to this treatment approach or to the optimal antibiotic regimen in this clinical situation.

    • Kim SJ, Scott IU, Brown GC, et al. Interventions for toxoplasma retinochoroiditis: a report by the American Academy of Ophthalmology. Ophthalmology. 2013;120(2): 371–378.

    • Kishore K, Conway MD, Peyman GA. Intravitreal clindamycin and dexamethasone for toxoplasmic retinochoroiditis. Ophthalmic Surg Lasers. 2001;32(3):183–192.

    • Silveira C, Belfort R Jr, Muccioli C, et al. The effect of long-term intermittent trimethoprim/sulfamethoxazole treatment on recurrences of toxoplasmic retinochoroiditis. Am J Ophthalmol. 2002;134(1):41–46.

    • Soheilian M, Ramezani A, Azimzadeh A, et al. Randomized trial of intravitreal clindamycin and dexamethasone versus pyrimethamine, sulfadiazine, and prednisolone in treatment of ocular toxoplasmosis. Ophthalmology 2011;118(1):134–141.

    • Soheilian M, Sadoughi MM, Ghajarnia M, et al. Prospective randomized trial of trimethoprim/sulfamethoxazole versus pyrimethamine and sulfadiazine in the treatment of ocular toxoplasmosis. Ophthalmology. 2005;112(11):1876–1882.

    Excerpted from BCSC 2020-2021 series: Section 9 - Uveitis and Ocular Inflammation. For more information and to purchase the entire series, please visit https://www.aao.org/bcsc.

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